PI(4,5)P2-binding effector proteins for vesicle exocytosis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 6, 2015, Pages 785-793

  Martin, Thomas F J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

CAPS CADPS; Munc13; Phosphatidylinositol(4,5)bisphosphate; SNARE protein; Synaptotagmin; Vesicle exocytosis

Indexed keywords

CALCIUM; CALCIUM BINDING PROTEIN; NERVE PROTEIN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN BINDING; SYNAPTOTAGMIN I; SYNTAXIN 1; VESICULAR TRANSPORT PROTEIN;

ANIMAL; CHEMISTRY; EXOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM-BINDING PROTEINS; EXOCYTOSIS; GENE EXPRESSION REGULATION; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN BINDING; SIGNAL TRANSDUCTION; SYNAPTOTAGMIN I; SYNTAXIN 1; TRANSPORT VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 84927648644     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.09.017     Document Type: Review

References (164)

1. R.W. Holz, M.A. Bittner, S.C. Peppers, R.A. Senter, and D.A. Eberhard MgATP-independent and MgATP-dependent exocytosis. Evidence that MgATP primes adrenal chromaffin cells to undergo exocytosis J. Biol. Chem. 264 1989 5412 5419
2. J.C. Hay, and T.F. Martin Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins J. Cell Biol. 119 1992 139 151
3. D.A. Eberhard, C.L. Cooper, M.G. Low, and R.W. Holz Evidence that the inositol phospholipids are necessary for exocytosis. Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP Biochem. J. 268 1990 15 25
4. J.C. Hay, and T.F. Martin Phosphatidylinositol transfer protein required for ATP-dependent priming of Ca(2 +)-activated secretion Nature 366 1993 572 575
5. J.C. Hay, P.L. Fisette, G.H. Jenkins, K. Fukami, T. Takenawa, R.A. Anderson, and T.F. Martin ATP-dependent inositide phosphorylation required for Ca(2 +)-activated secretion Nature 374 1995 173 177
6. R.W. Holz, M.D. Hlubek, S.D. Sorensen, S.K. Fisher, T. Balla, S. Ozaki, G.D. Prestwich, E.L. Stuenkel, and M.A. Bittner A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis J. Biol. Chem. 275 2000 17878 17885
7. R.N. Grishanin, J.A. Kowalchyk, V.A. Klenchin, K. Ann, C.A. Earles, E.R. Chapman, R.R. Gerona, and T.F. Martin CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein Neuron 43 2004 551 562
8. I. Milosevic, J.B. Sorensen, T. Lang, M. Krauss, G. Nagy, V. Haucke, R. Jahn, and E. Neher Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells J. Neurosci. Off. J. Soc. Neurosci. 25 2005 2557 2565
9. S. Debaisieux, F. Rayne, H. Yezid, and B. Beaumelle The ins and outs of HIV-1 Tat Traffic 13 2012 355 363
10. P. Tryoen-Toth, S. Chasserot-Golaz, A. Tu, P. Gherib, M.F. Bader, B. Beaumelle, and N. Vitale HIV-1 Tat protein inhibits neurosecretion by binding to phosphatidylinositol 4,5-bisphosphate J. Cell Sci. 126 2013 454 463
11. L.W. Gong, G. Di Paolo, E. Diaz, G. Cestra, M.E. Diaz, M. Lindau, P. De Camilli, and D. Toomre Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion Proc. Natl. Acad. Sci. U. S. A. 102 2005 5204 5209
12. Y. Aikawa, and T.F. Martin ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis J. Cell Biol. 162 2003 647 659
13. T.F. Martin, K.M. Loyet, V.A. Barry, and J.A. Kowalchyk The role of PtdIns(4,5)P2 in exocytotic membrane fusion Biochem. Soc. Trans. 25 1997 1137 1141
14. S. Chasserot-Golaz, P. Hubert, D. Thierse, S. Dirrig, C.J. Vlahos, D. Aunis, and M.F. Bader Possible involvement of phosphatidylinositol 3-kinase in regulated exocytosis: studies in chromaffin cells with inhibitor LY294002 J. Neurochem. 70 1998 2347 2356
15. T. Balla Phosphoinositides: tiny lipids with giant impact on cell regulation Physiol. Rev. 93 2013 1019 1137
16. H.L. Olsen, M. Hoy, W. Zhang, A.M. Bertorello, K. Bokvist, K. Capito, A.M. Efanov, B. Meister, P. Thams, S.N. Yang, P. Rorsman, P.O. Berggren, and J. Gromada Phosphatidylinositol 4-kinase serves as a metabolic sensor and regulates priming of secretory granules in pancreatic beta cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 5187 5192
17. T.F. Martin Role of PI(4,5)P(2) in vesicle exocytosis and membrane fusion Subcell. Biochem. 59 2012 111 130
18. L. Yakir-Tamang, and J.E. Gerst Phosphoinositides, exocytosis and polarity in yeast: all about actin? Trends Cell Biol. 19 2009 677 684
19. Y. Saheki, and P. De Camilli Synaptic vesicle endocytosis Cold Spring Harb. Perspect. Biol. 4 2012 a005645
20. S.E. Moss How actin gets the PIP Sci. Signal. 5 2012 e7
21. N.J. Schill, and R.A. Anderson Out, in and back again: PtdIns(4,5)P(2) regulates cadherin trafficking in epithelial morphogenesis Biochem. J. 418 2009 247 260
22. S. Grinstein Imaging signal transduction during phagocytosis: phospholipids, surface charge, and electrostatic interactions Am. J. Physiol. Cell Physiol. 299 2010 C876 C881
23. A. Alfadhli, and E. Barklis The roles of lipids and nucleic acids in HIV-1 assembly Front. Microbiol. 5 2014 253
24. P.A. Oude Weernink, M. Lopez de Jesus, and M. Schmidt Phospholipase D signaling: orchestration by PIP2 and small GTPases Naunyn Schmiedeberg's Arch. Pharmacol. 374 2007 399 411
25. B.C. Suh, and B. Hille Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate Curr. Opin. Neurobiol. 15 2005 370 378
26. M. Abe, A. Makino, F. Hullin-Matsuda, K. Kamijo, Y. Ohno-Iwashita, K. Hanada, H. Mizuno, A. Miyawaki, and T. Kobayashi A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol-4,5-bisphosphate to the cleavage furrow during cytokinesis Mol. Cell. Biol. 32 2012 1396 1407
27. R. Behnia, and S. Munro Organelle identity and the signposts for membrane traffic Nature 438 2005 597 604
28. T.G. Kutateladze Molecular analysis of protein-phosphoinositide interactions Curr. Top. Microbiol. Immunol. 362 2012 111 126
29. W. Cho, and R.V. Stahelin Membrane-protein interactions in cell signaling and membrane trafficking Annu. Rev. Biophys. Biomol. Struct. 34 2005 119 151
30. M.A. Lemmon Membrane recognition by phospholipid-binding domains. Nature reviews Mol. Cell Biol. 9 2008 99 111
31. R. Jahn, and D. Fasshauer Molecular machines governing exocytosis of synaptic vesicles Nature 490 2012 201 207
32. T.C. Sudhof Calcium control of neurotransmitter release Cold Spring Harb. Perspect. Biol. 4 2012 a011353
33. D.J. James, and T.F. Martin CAPS and Munc13: CATCHRs that SNARE vesicles Front. Endocrinol. 4 2013 187
34. M.R. Ammar, N. Kassas, S. Chasserot-Golaz, M.F. Bader, and N. Vitale Lipids in regulated exocytosis: what are they doing? Front. Endocrinol. 4 2013 125
35. M. Fukuda Rab27 effectors, pleiotropic regulators in secretory pathways Traffic 14 2013 949 963
36. M. Koch, and M. Holt Coupling exo- and endocytosis: an essential role for PIP(2) at the synapse Biochim. Biophys. Acta 1821 2012 1114 1132
37. T.C. Sudhof, and J. Rizo Synaptic vesicle exocytosis Cold Spring Harb. Perspect. Biol. 3 2011
38. P. Mayinger Phosphoinositides and vesicular membrane traffic Biochim. Biophys. Acta 1821 2012 1104 1113
39. J. Rizo, and T.C. Sudhof The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices - guilty as charged? Annu. Rev. Cell Dev. Biol. 28 2012 279 308
40. P.J. Wen, S.L. Osborne, and F.A. Meunier Dynamic control of neuroexocytosis by phosphoinositides in health and disease Prog. Lipid Res. 50 2011 52 61
41. O. Idevall-Hagren, E.J. Dickson, B. Hille, D.K. Toomre, and P. De Camilli Optogenetic control of phosphoinositide metabolism Proc. Natl. Acad. Sci. U. S. A. 109 2012 E2316 E2323
42. C. Schultz Challenges in studying phospholipid signaling Nat. Chem. Biol. 6 2010 473 475
43. M.J. Wakelam The uses and limitations of the analysis of cellular phosphoinositides by lipidomic and imaging methodologies Biochim. Biophys. Acta 1841 2014 1102 1107
44. T. Laux, K. Fukami, M. Thelen, T. Golub, D. Frey, and P. Caroni GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism J. Cell Biol. 149 2000 1455 1472
45. K. Fukami, K. Matsuoka, O. Nakanishi, A. Yamakawa, S. Kawai, and T. Takenawa Antibody to phosphatidylinositol 4,5-bisphosphate inhibits oncogene-induced mitogenesis Proc. Natl. Acad. Sci. U. S. A. 85 1988 9057 9061
46. K. Aoyagi, T. Sugaya, M. Umeda, S. Yamamoto, S. Terakawa, and M. Takahashi The activation of exocytotic sites by the formation of phosphatidylinositol 4,5-bisphosphate microdomains at syntaxin clusters J. Biol. Chem. 280 2005 17346 17352
47. D.J. James, C. Khodthong, J.A. Kowalchyk, and T.F. Martin Phosphatidylinositol 4,5-bisphosphate regulates SNARE-dependent membrane fusion J. Cell Biol. 182 2008 355 366
48. E. Umbrecht-Jenck, V. Demais, V. Calco, Y. Bailly, M.F. Bader, and S. Chasserot-Golaz S100A10-mediated translocation of annexin-A2 to SNARE proteins in adrenergic chromaffin cells undergoing exocytosis Traffic 11 2010 958 971
49. G. van den Bogaart, K. Meyenberg, H.J. Risselada, H. Amin, K.I. Willig, B.E. Hubrich, M. Dier, S.W. Hell, H. Grubmuller, U. Diederichsen, and R. Jahn Membrane protein sequestering by ionic protein-lipid interactions Nature 479 2011 552 555
50. J. Wang, and D.A. Richards Segregation of PIP2 and PIP3 into distinct nanoscale regions within the plasma membrane Biol. Open 1 2012 857 862
51. G. Kabachinski, M. Yamaga, D.M. Kielar-Grevstad, S. Bruinsma, and T.F. Martin CAPS and Munc13 utilize distinct PIP2-linked mechanisms to promote vesicle exocytosis Mol. Biol. Cell 25 2014 508 521
52. A.M. Sokac, and W.M. Bement Kiss-and-coat and compartment mixing: coupling exocytosis to signal generation and local actin assembly Mol. Biol. Cell 17 2006 1495 1502
53. L.J. Pike, and J.M. Miller Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover J. Biol. Chem. 273 1998 22298 22304
54. Y.H. Wang, D.R. Slochower, and P.A. Janmey Counterion-mediated cluster formation by polyphosphoinositides Chem. Phys. Lipids 182 2014 38 51
55. I.L. Salvemini, D.M. Gau, J. Reid, L.A. Bagatolli, A. Macmillan, and P.D. Moens Low PIP(2) molar fractions induce nanometer size clustering in giant unilamellar vesicles Chem. Phys. Lipids 177 2014 51 63
56. S. McLaughlin, and D. Murray Plasma membrane phosphoinositide organization by protein electrostatics Nature 438 2005 605 611
57. J. Nilsson, B. Persson, and G. von Heijne Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes Proteins 60 2005 606 616
58. M.A. Surma, C. Klose, and K. Simons Lipid-dependent protein sorting at the trans-Golgi network Biochim. Biophys. Acta 1821 2012 1059 1067
59. G.R. Hammond, M.J. Fischer, K.E. Anderson, J. Holdich, A. Koteci, T. Balla, and R.F. Irvine PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity Science 337 2012 727 730
60. Y. Sun, N. Thapa, A.C. Hedman, and R.A. Anderson Phosphatidylinositol 4,5-bisphosphate: targeted production and signaling Bioessays News Rev. Mol. Cell. Dev. Biol. 35 2013 513 522
61. K. Kwiatkowska One lipid, multiple functions: how various pools of PI(4,5)P(2) are created in the plasma membrane Cell Mol. Life Sci. CMLS 67 2010 3927 3946
62. G.D. Fairn, K. Ogata, R.J. Botelho, P.D. Stahl, R.A. Anderson, P. De Camilli, T. Meyer, S. Wodak, and S. Grinstein An electrostatic switch displaces phosphatidylinositol phosphate kinases from the membrane during phagocytosis J. Cell Biol. 187 2009 701 714
63. N. Vitale, S. Chasserot-Golaz, Y. Bailly, N. Morinaga, M.A. Frohman, and M.F. Bader Calcium-regulated exocytosis of dense-core vesicles requires the activation of ADP-ribosylation factor (ARF)6 by ARF nucleotide binding site opener at the plasma membrane J. Cell Biol. 159 2002 79 89
64. M.R. Wenk, L. Pellegrini, V.A. Klenchin, G. Di Paolo, S. Chang, L. Daniell, M. Arioka, T.F. Martin, and P. De Camilli PIP kinase Igamma is the major PI(4,5)P(2) synthesizing enzyme at the synapse Neuron 32 2001 79 88
65. J.R. Morgan, G. Di Paolo, H. Werner, V.A. Shchedrina, M. Pypaert, V.A. Pieribone, and P. De Camilli A role for talin in presynaptic function J. Cell Biol. 167 2004 43 50
66. G. Di Paolo, L. Pellegrini, K. Letinic, G. Cestra, R. Zoncu, S. Voronov, S. Chang, J. Guo, M.R. Wenk, and P. De Camilli Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin Nature 420 2002 85 89
67. K. Ling, R.L. Doughman, A.J. Firestone, M.W. Bunce, and R.A. Anderson Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions Nature 420 2002 89 93
68. M. Krauss, V. Kukhtina, A. Pechstein, and V. Haucke Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2mu-cargo complexes Proc. Natl. Acad. Sci. U. S. A. 103 2006 11934 11939
69. X. Xiong, Q. Xu, Y. Huang, R.D. Singh, R. Anderson, E. Leof, J. Hu, and K. Ling An association between type Igamma PI4P 5-kinase and Exo70 directs E-cadherin clustering and epithelial polarization Mol. Biol. Cell 23 2012 87 98
70. K. Carvalho, L. Ramos, C. Roy, and C. Picart Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: characterization and functionality Biophys. J. 95 2008 4348 4360
71. T. Lang, D. Bruns, D. Wenzel, D. Riedel, P. Holroyd, C. Thiele, and R. Jahn SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis EMBO J. 20 2001 2202 2213
72. J.J. Sieber, K.I. Willig, R. Heintzmann, S.W. Hell, and T. Lang The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane Biophys. J. 90 2006 2843 2851
73. J.J. Sieber, K.I. Willig, C. Kutzner, C. Gerding-Reimers, B. Harke, G. Donnert, B. Rammner, C. Eggeling, S.W. Hell, H. Grubmuller, and T. Lang Anatomy and dynamics of a supramolecular membrane protein cluster Science 317 2007 1072 1076
74. C. Rickman, C.N. Medine, A.R. Dun, D.J. Moulton, O. Mandula, N.D. Halemani, S.O. Rizzoli, L.H. Chamberlain, and R.R. Duncan t-SNARE protein conformations patterned by the lipid microenvironment J. Biol. Chem. 285 2010 13535 13541
75. S. Barg, M.K. Knowles, X. Chen, M. Midorikawa, and W. Almers Syntaxin clusters assemble reversibly at sites of secretory granules in live cells Proc. Natl. Acad. Sci. U. S. A. 107 2010 20804 20809
76. M.K. Knowles, S. Barg, L. Wan, M. Midorikawa, X. Chen, and W. Almers Single secretory granules of live cells recruit syntaxin-1 and synaptosomal associated protein 25 (SNAP-25) in large copy numbers Proc. Natl. Acad. Sci. U. S. A. 107 2010 20810 20815
77. N.R. Gandasi, and S. Barg Contact-induced clustering of syntaxin and munc18 docks secretory granules at the exocytosis site Nat. Commun. 5 2014 3914
78. 2 + induces clustering of membrane proteins in the plasma membrane via electrostatic interactions EMBO J. 30 2011 1209 1220
79. D. Bar-On, S. Wolter, S. van de Linde, M. Heilemann, G. Nudelman, E. Nachliel, M. Gutman, M. Sauer, and U. Ashery Super-resolution imaging reveals the internal architecture of nano-sized syntaxin clusters J. Biol. Chem. 287 2012 27158 27167
80. A. Honigmann, G. van den Bogaart, E. Iraheta, H.J. Risselada, D. Milovanovic, V. Mueller, S. Mullar, U. Diederichsen, D. Fasshauer, H. Grubmuller, S.W. Hell, C. Eggeling, K. Kuhnel, and R. Jahn Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment Nat. Struct. Mol. Biol. 20 2013 679 686
81. T.M. Khuong, R.L. Habets, S. Kuenen, A. Witkowska, J. Kasprowicz, J. Swerts, R. Jahn, G. van den Bogaart, and P. Verstreken Synaptic PI(3,4,5)P3 is required for Syntaxin1A clustering and neurotransmitter release Neuron 77 2013 1097 1108
82. A. Pertsinidis, K. Mukherjee, M. Sharma, Z.P. Pang, S.R. Park, Y. Zhang, A.T. Brunger, T.C. Sudhof, and S. Chu Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ Proc. Natl. Acad. Sci. U. S. A. 110 2013 E2812 E2820
83. M.L. Wagner, and L.K. Tamm Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers Biophys. J. 81 2001 266 275
84. L. Yang, A.R. Dun, K.J. Martin, Z. Qiu, A. Dunn, G.J. Lord, W. Lu, R.R. Duncan, and C. Rickman Secretory vesicles are preferentially targeted to areas of low molecular SNARE density PLoS One 7 2012 e49514
85. G. van den Bogaart, T. Lang, and R. Jahn Microdomains of SNARE proteins in the plasma membrane Curr. Top. Membr. 72 2013 193 230
86. I. Lopez, J.A. Ortiz, J. Villanueva, V. Torres, C.J. Torregrosa-Hetland, M. del Mar Frances, S. Viniegra, and L.M. Gutierrez Vesicle motion and fusion are altered in chromaffin cells with increased SNARE cluster dynamics Traffic 10 2009 172 185
87. D.H. Murray, and L.K. Tamm Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol Biochemistry 48 2009 4617 4625
88. D.H. Murray, and L.K. Tamm Molecular mechanism of cholesterol- and polyphosphoinositide-mediated syntaxin clustering Biochemistry 50 2011 9014 9022
89. A.D. Lam, P. Tryoen-Toth, B. Tsai, N. Vitale, and E.L. Stuenkel SNARE-catalyzed fusion events are regulated by Syntaxin1A-lipid interactions Mol. Biol. Cell 19 2008 485 497
90. 2 +-dependent activator protein for secretion) with the three neuronal SNARE proteins required for vesicle fusion J. Biol. Chem. 285 2010 35320 35329
91. D.H. Kweon, C.S. Kim, and Y.K. Shin Insertion of the membrane-proximal region of the neuronal SNARE coiled coil into the membrane J. Biol. Chem. 278 2003 12367 12373
92. J.S. Van Komen, X. Bai, T.L. Rodkey, J. Schaub, and J.A. McNew The polybasic juxtamembrane region of Sso1p is required for SNARE function in vivo Eukaryot. Cell 4 2005 2017 2028
93. F.A. Meunier, S.L. Osborne, G.R. Hammond, F.T. Cooke, P.J. Parker, J. Domin, and G. Schiavo Phosphatidylinositol 3-kinase C2alpha is essential for ATP-dependent priming of neurosecretory granule exocytosis Mol. Biol. Cell 16 2005 4841 4851
94. P.J. Wen, S.L. Osborne, M. Zanin, P.C. Low, H.T. Wang, S.M. Schoenwaelder, S.P. Jackson, R. Wedlich-Soldner, B. Vanhaesebroeck, D.J. Keating, and F.A. Meunier Phosphatidylinositol(4,5)bisphosphate coordinates actin-mediated mobilization and translocation of secretory vesicles to the plasma membrane of chromaffin cells Nat. Commun. 2 2011 491
95. T. Nishizaki, J.H. Walent, J.A. Kowalchyk, and T.F. Martin A key role for a 145-kDa cytosolic protein in the stimulation of Ca(2 +)-dependent secretion by protein kinase C J. Biol. Chem. 267 1992 23972 23981
96. J.H. Walent, B.W. Porter, and T.F. Martin A novel 145 kd brain cytosolic protein reconstitutes Ca(2 +)-regulated secretion in permeable neuroendocrine cells Cell 70 1992 765 775
97. 2 +-activated exocytosis J. Biol. Chem. 272 1997 19637 19640
98. 2 +-dependent exocytosis J. Biol. Chem. 277 2002 22025 22034
99. K.M. Loyet, J.A. Kowalchyk, A. Chaudhary, J. Chen, G.D. Prestwich, and T.F. Martin Specific binding of phosphatidylinositol 4,5-bisphosphate to calcium-dependent activator protein for secretion (CAPS), a potential phosphoinositide effector protein for regulated exocytosis J. Biol. Chem. 273 1998 8337 8343
100. D.J. James, J. Kowalchyk, N. Daily, M. Petrie, and T.F. Martin CAPS drives trans-SNARE complex formation and membrane fusion through syntaxin interactions Proc. Natl. Acad. Sci. U. S. A. 106 2009 17308 17313
101. 2 + regulator of synaptic exocytosis Nat. Struct. Mol. Biol. 17 2010 280 288
102. N. Brose, A. Betz, and H. Wegmeyer Divergent and convergent signaling by the diacylglycerol second messenger pathway in mammals Curr. Opin. Neurobiol. 14 2004 328 340
103. N. Lipstein, T. Sakaba, B.H. Cooper, K.H. Lin, N. Strenzke, U. Ashery, J.S. Rhee, H. Taschenberger, E. Neher, and N. Brose Dynamic control of synaptic vesicle replenishment and short-term plasticity by Ca(2 +)-calmodulin-Munc13-1 signaling Neuron 79 2013 82 96
104. S.G. Frere, B. Chang-Ileto, and G. Di Paolo Role of phosphoinositides at the neuronal synapse Subcell. Biochem. 59 2012 131 175
105. X. Zhang, X. Chen, C. Jia, X. Geng, X. Du, and H. Zhang Depolarization increases phosphatidylinositol (PI) 4,5-bisphosphate level and KCNQ currents through PI 4-kinase mechanisms J. Biol. Chem. 285 2010 9402 9409
106. X. Wang, B. Hu, A. Zieba, N.G. Neumann, M. Kasper-Sonnenberg, A. Honsbein, G. Hultqvist, T. Conze, W. Witt, C. Limbach, M. Geitmann, H. Danielson, R. Kolarow, G. Niemann, V. Lessmann, and M.W. Kilimann A protein interaction node at the neurotransmitter release site: domains of Aczonin/Piccolo, Bassoon, CAST, and rim converge on the N-terminal domain of Munc13-1 J. Neurosci. Off. J. Soc. Neurosci. 29 2009 12584 12596
107. Y.S. Andrews-Zwilling, H. Kawabe, K. Reim, F. Varoqueaux, and N. Brose Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2 J. Biol. Chem. 281 2006 19720 19731
108. S. Kalla, M. Stern, J. Basu, F. Varoqueaux, K. Reim, C. Rosenmund, N.E. Ziv, and N. Brose Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice J. Neurosci. Off. J. Soc. Neurosci. 26 2006 13054 13066
109. C. Ma, L. Su, A.B. Seven, Y. Xu, and J. Rizo Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release Science 339 2013 421 425
110. U. Ashery, F. Varoqueaux, T. Voets, A. Betz, P. Thakur, H. Koch, E. Neher, N. Brose, and J. Rettig Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells EMBO J. 19 2000 3586 3596
111. R. Friedrich, I. Gottfried, and U. Ashery Munc13-1 translocates to the plasma membrane in a Doc2B- and calcium-dependent manner Front. Endocrinol. 4 2013 119
112. E. Oancea, and T. Meyer Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals Cell 95 1998 307 318
113. 2 +-dependent exocytotic machinery J. Biol. Chem. 272 1997 16081 16084
114. 2 + sensor for spontaneous neurotransmitter release Science 327 2010 1614 1618
115. E.A. Nalefski, and J.J. Falke The C2 domain calcium-binding motif: structural and functional diversity Protein Sci. Publ. Protein Soc. 5 1996 2375 2390
116. 2 +-binding domain J. Biol. Chem. 273 1998 15879 15882
117. R. Friedrich, A. Yeheskel, and U. Ashery DOC2B, C2 domains, and calcium: a tale of intricate interactions Mol. Neurobiol. 41 2010 42 51
118. S. Corbalan-Garcia, and J.C. Gomez-Fernandez Signaling through C2 domains: more than one lipid target Biochim. Biophys. Acta 1838 2014 1536 1547
119. E.R. Chapman How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77 2008 615 641
120. 2 + and PI(4,5)P2 binding modes of the C2 domains of rabphilin 3A and synaptotagmin 1 Proc. Natl. Acad. Sci. U. S. A. 110 2013 20503 20508
121. J. Bai, W.C. Tucker, and E.R. Chapman PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane Nat. Struct. Mol. Biol. 11 2004 36 44
122. G. Schiavo, Q.M. Gu, G.D. Prestwich, T.H. Sollner, and J.E. Rothman Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin Proc. Natl. Acad. Sci. U. S. A. 93 1996 13327 13332
123. 2 + affinity of synaptotagmin 1 is markedly increased by a specific interaction of its C2B domain with phosphatidylinositol 4,5-bisphosphate J. Biol. Chem. 284 2009 25749 25760
124. W. Kuo, D.Z. Herrick, and D.S. Cafiso Phosphatidylinositol 4,5-bisphosphate alters synaptotagmin 1 membrane docking and drives opposing bilayers closer together Biochemistry 50 2011 2633 2641
125. 2 + affinity of synaptotagmin-1 by 40-fold J. Biol. Chem. 287 2012 16447 16453
126. 2 + binding to C2 domains of synaptotagmin 1 J. Biol. Chem. 281 2006 15845 15852
127. 2 +-independent stage of synaptic vesicle priming in vivo Mol. Biol. Cell 17 2006 5211 5226
128. Z. Wang, H. Liu, Y. Gu, and E.R. Chapman Reconstituted synaptotagmin I mediates vesicle docking, priming, and fusion J. Cell Biol. 195 2011 1159 1170
129. A.B. Seven, K.D. Brewer, L. Shi, Q.X. Jiang, and J. Rizo Prevalent mechanism of membrane bridging by synaptotagmin-1 Proc. Natl. Acad. Sci. U. S. A. 110 2013 E3243 E3252
130. E. Hui, J.D. Gaffaney, Z. Wang, C.P. Johnson, C.S. Evans, and E.R. Chapman Mechanism and function of synaptotagmin-mediated membrane apposition Nat. Struct. Mol. Biol. 18 2011 813 821
131. E. Connell, A. Giniatullina, J. Lai-Kee-Him, R. Tavare, E. Ferrari, A. Roseman, D. Cojoc, A.R. Brisson, and B. Davletov Cross-linking of phospholipid membranes is a conserved property of calcium-sensitive synaptotagmins J. Mol. Biol. 380 2008 42 50
132. G. van den Bogaart, S. Thutupalli, J.H. Risselada, K. Meyenberg, M. Holt, D. Riedel, U. Diederichsen, S. Herminghaus, H. Grubmuller, and R. Jahn Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation Nat. Struct. Mol. Biol. 18 2011 805 812
133. U.B. Choi, P. Strop, M. Vrljic, S. Chu, A.T. Brunger, and K.R. Weninger Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex Nat. Struct. Mol. Biol. 17 2010 318 324
134. A.L. Lai, H. Huang, D.Z. Herrick, N. Epp, and D.S. Cafiso Synaptotagmin 1 and SNAREs form a complex that is structurally heterogeneous J. Mol. Biol. 405 2011 696 706
135. 2 +-triggered vesicle fusion Nat. Struct. Mol. Biol. 17 2010 325 331
136. J. Tang, A. Maximov, O.H. Shin, H. Dai, J. Rizo, and T.C. Sudhof A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis Cell 126 2006 1175 1187
137. 2 + drive trans SNARE zippering Sci. Rep. 4 2014 4575
138. 2 +-triggered vesicle exocytosis Mol. Biol. Cell 18 2007 4957 4968
139. C. Rickman, D.A. Archer, F.A. Meunier, M. Craxton, M. Fukuda, R.D. Burgoyne, and B. Davletov Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate J. Biol. Chem. 279 2004 12574 12579
140. 2 +-phospholipid complex in neurotransmitter release J. Mol. Biol. 367 2007 848 863
141. S.L. Osborne, T.P. Wallis, J.L. Jimenez, J.J. Gorman, and F.A. Meunier Identification of secretory granule phosphatidylinositol 4,5-bisphosphate-interacting proteins using an affinity pulldown strategy Mol. Cell Proteomics MCP 6 2007 1158 1169
142. K.L. Boswell, D.J. James, J.M. Esquibel, S. Bruinsma, R. Shirakawa, H. Horiuchi, and T.F. Martin Munc13-4 reconstitutes calcium-dependent SNARE-mediated membrane fusion J. Cell Biol. 197 2012 301 312
143. M. Sato, Y. Mori, T. Matsui, R. Aoki, M. Oya, Y. Yanagihara, M. Fukuda, and T. Tsuboi Role of the polybasic sequence in the Doc2alpha C2B domain in dense-core vesicle exocytosis in PC12 cells J. Neurochem. 114 2010 171 181
144. T.A. Lyakhova, and J.D. Knight The C2 domains of granuphilin are high-affinity sensors for plasma membrane lipids Chem. Phys. Lipids 182 2014 29 37
145. P. Novick, S. Ferro, and R. Schekman Order of events in the yeast secretory pathway Cell 25 1981 461 469
146. D.R. TerBush, T. Maurice, D. Roth, and P. Novick The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae EMBO J. 15 1996 6483 6494
147. S.C. Hsu, A.E. Ting, C.D. Hazuka, S. Davanger, J.W. Kenny, Y. Kee, and R.H. Scheller The mammalian brain rsec6/8 complex Neuron 17 1996 1209 1219
148. M.R. Heider, and M. Munson Exorcising the exocyst complex Traffic 13 2012 898 907
149. M. Inoue, L. Chang, J. Hwang, S.H. Chiang, and A.R. Saltiel The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin Nature 422 2003 629 633
150. C. Boyd, T. Hughes, M. Pypaert, and P. Novick Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p J. Cell Biol. 167 2004 889 901
151. F. Morgera, M.R. Sallah, M.L. Dubuke, P. Gandhi, D.N. Brewer, C.M. Carr, and M. Munson Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1 Mol. Biol. Cell 23 2012 337 346
152. I.M. Yu, and F.M. Hughson Tethering factors as organizers of intracellular vesicular traffic Annu. Rev. Cell Dev. Biol. 26 2010 137 156
153. C. Brocker, S. Engelbrecht-Vandre, and C. Ungermann Multisubunit tethering complexes and their role in membrane fusion Curr. Biol. CB 20 2010 R943 R952
154. M. Munson, and P. Novick The exocyst defrocked, a framework of rods revealed Nat. Struct. Mol. Biol. 13 2006 577 581
155. M.V. Sivaram, M.L. Furgason, D.N. Brewer, and M. Munson The structure of the exocyst subunit Sec6p defines a conserved architecture with diverse roles Nat. Struct. Mol. Biol. 13 2006 555 556
156. W. Li, C. Ma, R. Guan, Y. Xu, D.R. Tomchick, and J. Rizo The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors Structure 19 2011 1443 1455
157. X. Zhang, K. Orlando, B. He, F. Xi, J. Zhang, A. Zajac, and W. Guo Membrane association and functional regulation of Sec3 by phospholipids and Cdc42 J. Cell Biol. 180 2008 145 158
158. B. He, F. Xi, X. Zhang, J. Zhang, and W. Guo Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane EMBO J. 26 2007 4053 4065
159. K. Baek, A. Knodler, S.H. Lee, X. Zhang, K. Orlando, J. Zhang, T.J. Foskett, W. Guo, and R. Dominguez Structure-function study of the N-terminal domain of exocyst subunit Sec3 J. Biol. Chem. 285 2010 10424 10433
160. M. Yamashita, K. Kurokawa, Y. Sato, A. Yamagata, H. Mimura, A. Yoshikawa, K. Sato, A. Nakano, and S. Fukai Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3 Nat. Struct. Mol. Biol. 17 2010 180 186
161. J. Liu, X. Zuo, P. Yue, and W. Guo Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells Mol. Biol. Cell 18 2007 4483 4492
162. T. Strahl, and J. Thorner Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae Biochim. Biophys. Acta 1771 2007 353 404
163. Y. Zhao, J. Liu, C. Yang, B.R. Capraro, T. Baumgart, R.P. Bradley, N. Ramakrishnan, X. Xu, R. Radhakrishnan, T. Svitkina, and W. Guo Exo70 generates membrane curvature for morphogenesis and cell migration Dev. Cell 26 2013 266 278
164. N. Thapa, and R.A. Anderson PIP2 signaling, an integrator of cell polarity and vesicle trafficking in directionally migrating cells Cell Adhes. Migr. 6 2012 409 412